Segregation of Lolium perenne into a subpopulation with high infection by endophyte Epichloë festucae var. lolii results in improved agronomic performance

  • Zhenjiang Chen
  • Chunjie LiEmail author
  • Zhibiao Nan
  • James F. White
  • Yuanyuan Jin
  • Xuekai Wei
Regular Article


Background and aims

Low temperature stress is a common hazard during plant growth. Endophyte infection has been shown to increase cold tolerance in host plants. Many Lolium perenne cultivars contain low to moderate levels of endophyte. This study was done to explore cultivar improvement by segregation of endophyte containing individuals from the original cultivar to create a high endophyte subpopulation.


Endophyte-infected plants were segregated over the first 3 years to produce high-endophyte subpopulation, and field and greenhouse experiments were carried out in the forth and fifth to determine the cold tolerance of the L. perenne subpopulation with high endophyte infection rates (N), the parent (F), the control endophyte-free subpopulation (E) and the control local variety (L).


(1) After 3 years of screening, high endophyte infection rates in the tillers and seeds of plants were still observed (96.5%), and agronomic traits (crown width, plant height, panicle number, withering, regreen-up, the growth cycle and the over-wintering rate) was also improved with increased Epichloë colonization of host plant. (2) The subpopulation with high endophyte infection rates and improved agronomic traits had better cold tolerance than the parent, the control endophyte-free subpopulation and the control local variety. The possible mechanisms by which high endophyte infection enhances cold resistance in the field include increased root system, increased the over-wintering rate, reduced regrowth periods with the sowing date being October 15th. (3) The high-endophyte subpopulation significantly increased SOD, POD, CAT, and APX activities at 0, 5, and 10 °C by 11.8%–44.6%, compared with the parent population.


The subpopulation had a high endophyte infection rate, improved agronomic traits and higher enzymatic activities. These results indicate that increasing endophyte infection rates by selection, effectively improved agronomic traits and cold tolerance.


Lolium perenne E. festucae var. lolii Endophyte infection rate Cold tolerance Sowing date Low temperature stress 



We thank Jingle Zhou, Jing Liu, Hao Chen, and Weihu Lin for help with this experiments, and Taixiang Chen and Xiang Yao for beneficial discussions regarding the manuscript.

Funding information

This research was supported by the National Basic Research Program of China (2014CB138702), the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (2019QZKK0302), the Strategic Priority Research Program of Chinese Academy of Sciences (XDA20100102), Program for Changjiang Scholars and Innovative Research Team in University, China (IRT17R50), Fundamental Research Funds for the Central Universities (LZUJBKY-2018-kb10 and 2019-kb10) and 111 Project (B12002). The authors are thankful for support from USDA-NIFA Multistate Project W4147, and the New Jersey Agricultural Experiment Station.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.


  1. Barakat MN, Aldoss AA, Elshafei AA, Ghazy AI, Moustafa KA (2013) Assessment of genetic diversity among wheat doubled haploid plants using TRAP markers and morpho-agronomic traits. Aust J Crop Sci 7:104–111. CrossRefGoogle Scholar
  2. Barnawal D, Bharti N, Tripathi A, Pandey SS, Chanotiya CS, Kalra A (2016) ACC-deaminase-producing endophyte brachybacterium paraconglomeratum strain SMR20 ameliorates chlorophytum salinity stress via altering phytohormone generation. J Plant Growth Regul 35:1–12. CrossRefGoogle Scholar
  3. Barrero-Gil J, Huertas R, Rambla JL, Granell A, Salinas J (2016) Tomato plants increase their tolerance to low temperature in a chilling acclimation process entailing comprehensive transcriptional and metabolic adjustments. Plant Cell Environ 39:2303–2318. CrossRefPubMedGoogle Scholar
  4. Bhowmik PK, Tamura K, Sanada Y, Yamada T (2006) Sucrose metabolism of perennial ryegrass in relation to cold acclimation. Z Naturforsch C 61:99–104. CrossRefPubMedGoogle Scholar
  5. Bilska A, Sowiński P (2010) Closure of plasmodesmata in maize (Zea mays) at low temperature: a new mechanism for inhibition of photosynthesis. Ann Bot 106:675–686. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Brem D, Leuchtmann A (2010) Intraspecific competition of endophyte infected vs uninfected plants of two woodland grass species. Oikos 96:281–290. CrossRefGoogle Scholar
  7. Brulebabel AL, Fowler DB (1989) Use of controlled environments for winter cereal cold hardiness evslua. Can J Plant Sci 69:355–366. CrossRefGoogle Scholar
  8. Casler MD, Santen EV (2008) Fungal endophyte removal does not reduce cold tolerance of tall fescue. Crop Sci 48:2033–2039. CrossRefGoogle Scholar
  9. Chadha N, Mishra M, Rajpal K, Bajaj R, Choudhary DK, Varma A (2015) An ecological role of fungal endophytes to ameliorate plants under biotic stress. Arch Microbiol 197:869–881. CrossRefPubMedGoogle Scholar
  10. Chen N (2008) Genetic diversity of drunken horse grass (Achnatherum inebrians) and effects of its endophyte infection on cold tolerance. Thesis (Ph.D.): LanZhou University. (In Chinese, with English abstract)Google Scholar
  11. Chen Y, Jiang JF, Chang QC, Gu CS, Song AP, Chen SM, Dong B, Chen FD (2014) Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species. Mol Biol Rep 41:815–822. CrossRefPubMedGoogle Scholar
  12. Chen N, He RL, Chai Q, Li CJ, Nan ZB (2016) Transcriptomic analyses giving insights into molecular regulation mechanisms involved in cold tolerance by Epichloë endophyte in seed germination of Achnatherum inebrians. Plant Growth Regul 80:367–375. CrossRefGoogle Scholar
  13. Chen ZJ, Wei XK, Ying C, Tian P, Zhao XJ, Li CJ (2017) Research progress of methods on grass fungal endophyte detection. Pratacult Sci 11:1419–1433 (In Chinese, with English abstract)Google Scholar
  14. Chen TX, Johnson R, Chen SH, Lv H, Zhou JL, Li CJ (2018a) Infection by the fungal endophyte Epichloë bromicola enhances the tolerance of wild barley (Hordeum brevisubulatum) to salt and alkali stresses. Plant Soil 428:1–18. CrossRefGoogle Scholar
  15. Chen ZJ, Chen H, Wei XK, Tian P, Li CJ, Nan ZB (2018b) Screening of individual plants of Lolium perenne with high endophyte infection rate.10th International Symposium on Fungal Endophytes of Grasses: Book of abstracts 77.
  16. Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genetics Biology Fg B 45:84–93. CrossRefPubMedGoogle Scholar
  17. Clarke HJ, Siddique K (2004) Response of chickpea genotypes to low temperature stress during reproductive development. Field Crop Res 90:323–334. CrossRefGoogle Scholar
  18. Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127. CrossRefPubMedGoogle Scholar
  19. Conover MR (2003) Impact of the consumption of endophyte-infected perennial ryegrass by meadow voles. Agric Ecosyst Environ 97:199–203. CrossRefGoogle Scholar
  20. Dadkhah A (2008) Response of root yield and quality of sugar beet (Beta vulgaris) to salt stress. Comp Biochem Physiol 150:S196–S203. CrossRefGoogle Scholar
  21. Dalmannsdottir S, Jørgensen M, Rapacz M, Østrem L, Larsen A, Rødven R, Rognli OA (2017) Cold acclimation in warmer extended autumns impairs freezing tolerance of perennial ryegrass (Lolium perenne) and timothy (Phleum pratense). Physiol Plant 160:266–281. CrossRefPubMedGoogle Scholar
  22. Faltusová-Kadlecová Z, Faltus M, Prášil I (2002) Comparison of barley response to short-Term cold or dehydration. Biol Plantarum (Prague) 45:637–639. CrossRefGoogle Scholar
  23. Florea S, Schardl CL, Hollin W (2015) Detection and isolation of Epichloë species, fungal endophytes of grasses. Curr Protoc Microbiol 38:19A.1–19A24. CrossRefGoogle Scholar
  24. Garcíalara S, Arnason JT, Díazpontones D, Gonzalez E, Bergvinson DJ (2007) Soluble peroxidase activity in maize endosperm associated with maize weevil resistance. Crop Sci 47:1125–1130. CrossRefGoogle Scholar
  25. Gómez LD, Vanacker H, Buchner P, Noctor G, Foyer CH (2004) Intercellular distribution of glutathione synthesis in maize leaves and its response to short-term chilling. Plant Physiol 134:1662–1671. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gundel PE, Rudgers JA, Whitney KD (2017) Vertically transmitted symbionts as mechanisms of transgenerational effects. Am J Bot 104:787–792. CrossRefPubMedGoogle Scholar
  27. Hamilton CE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers 54:1–10. CrossRefGoogle Scholar
  28. Han H, Han B (2015) Evaluation of cold resistance and selection of chill-proof measure of three Phlox cultivars. J Anim Plant Sci 25:208–212Google Scholar
  29. Hashempour A, Ghasemnezhad M, Ghazvini RF, Sohani M (2014) Olive (Olea europaea L.) freezing tolerance related to antioxidant enzymes activity during cold acclimation and non acclimation. Acta Physiol Plant 36:3231–3241. CrossRefGoogle Scholar
  30. Hennessy LM, Popay AJ, Finch SC, Clearwater MJ, Cave VM (2016) Temperature and plant genotype alter alkaloid concentrations in ryegrass infected with an Epichloë endophyte and this affects an insect herbivore. Front Plant Sci 7:1907–1917. CrossRefGoogle Scholar
  31. Herd S, Christensen MJ, Saunders K, Scott DB, Schmid J (1997) Quantitative assessment of in planta distribution of metabolic activity and gene expression of an endophytic fungus. Microbiology 143:267–275. CrossRefPubMedGoogle Scholar
  32. Hill NS, Stringer WC, Rottinghaus GE, Belesky DP, Parrott WA, Pope DD (1990) Growth, morphological and chemical component responses of tall fescue to Acremonium coenophialum. Crop Sci 30:239–255 cs/abstracts/30/1/CS0300010156 CrossRefGoogle Scholar
  33. Huang CP, Qin NN, Sun L, Yu MY, Hu WZ, Qi ZY (2018) Selenium improves physiological parameters and alleviates oxidative stress in strawberry seedlings under low-temperature stress. Int J Mol Sci 19:1913–1926. CrossRefPubMedCentralGoogle Scholar
  34. Hume DE, Cooper BM, Panckhurst KA (2009) The role of endophyte in determining the persistence and productivity of ryegrass, tall fescue and meadow fescue in Northland. Proc N Z Grassl Assoc 71:145–150Google Scholar
  35. Hume DE, Roodi D, Mcgill CR, Millner JP, Johnson RD (2015) Beneficial endophytic microorganisms of Brassica – A review. Biol Control 90:102–112. CrossRefGoogle Scholar
  36. Hund A (2010) Genetic variation in the gravitropic response of maize roots to low temperatures. Plant Roots 4:22–30. CrossRefGoogle Scholar
  37. Hund A, Fracheboud Y, Soldati A, Stamp P (2008) Cold tolerance of maize seedlings as determined by root morphology and photosynthetic traits. Eur J Agron 28:178–185. CrossRefGoogle Scholar
  38. İşeri ÖD, Körpe DA, Sahin FI, Haberal M (2013) Hydrogen peroxide pretreatment of roots enhanced oxidative stress response of tomato under cold stress. Acta Physiol Plant 35:1905–1913. CrossRefGoogle Scholar
  39. Jha UC, Bohra A, Jha R (2017) Breeding approaches and genomics technologies to increase crop yield under low-temperature stress. Plant Cell Rep 36:1–35. CrossRefPubMedGoogle Scholar
  40. Kang GZ, Wang CH, Sun GC, Wang ZX (2003) Salicylic acid changes activities of H2O2-metabolizing enzymes and increases the chilling tolerance of banana seedlings. Environ Exp Bot 50:9–15. CrossRefGoogle Scholar
  41. Kari S, Gundel PE, Marjo H (2013) Chemical ecology mediated by fungal endophytes in grasses. J Chem Ecol 39:962–968. CrossRefGoogle Scholar
  42. Kelemu S, Cardona C, Segura G (2004) Antimicrobial and insecticidal protein isolated from seeds of Clitoria ternatea, a tropical forage legume. Plant Physiol Biochem 42:867–873. CrossRefPubMedGoogle Scholar
  43. Kong LY, Yan H, Bao YS, Chen HL (2012) Remote sensor monitoring method for winter wheat growth based on key development periods. Chin J Agrometeorol 33:424–430 (In Chinese, with English abstract)Google Scholar
  44. Kover PX, Dolan TE, Clay K (1997) Potential versus actual contribution of vertical transmission to pathogen fitness. P Royl Soc B Biol Sci 264:903–909. CrossRefGoogle Scholar
  45. Kovi MR, Fjellheim S, Sandve SR, Larsen A, Rudi H, Asp T, Kent MP, Rognli OA (2015) Population structure, genetic variation, and linkage disequilibrium in perennial ryegrass populations divergently selected for freezing tolerance. Front Plant Sci 6:929–942. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Lee DH, Lee CB (2000) Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci 59:75–85. CrossRefGoogle Scholar
  47. Lee BH, Lee HJ, Xiong LM, Zhu JK (2002) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14:1235–1251. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Lee SE, Hwang HJ, Ha JS, Jeong HS, Kim JH (2003) Screening of medicinal plant extracts for antioxidant activity. Life Sci 73:167–179. CrossRefPubMedGoogle Scholar
  49. Leuchtmann A, Bacon CW, Schardl CL, White JF, Tadych M (2014) Nomenclatural realignment of Neotyphodium species with genus Epicholë. Mycologia 106:202–215. CrossRefPubMedGoogle Scholar
  50. Li BQ, Zhang CF, Cao BH, Qin GZ, Wang WH, Tian SP (2012) Brassinolide enhances cold stress tolerance of fruit by regulating plasma membrane proteins and lipids. Amino Acids 43:2469–2480. CrossRefPubMedGoogle Scholar
  51. Liu CH, Yu D (2009) The bud and root sprouting capacity of Alternanthera philoxeroides after over-wintering on sediments of a drained canal. Hydrobiologia 623:251–256. CrossRefGoogle Scholar
  52. Liu BY, Lei CY, Shu T, Zhang YS, Jin JH, Li S, Liu WQ (2015) Effects of low-temperature stress on secondary metabolism in mosses exposed to simulated N deposition. Trans Bot Soc Edinburgh 8:415–426. CrossRefGoogle Scholar
  53. Lukatkin AS (2002) Contribution of oxidative stress to the development of cold-induced damage to leaves of chilling-sensitive plants: 2. The Activity of Antioxidant Enzymes during Plant Chilling. Russ J Plant Physhl 49:782–788. CrossRefGoogle Scholar
  54. Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiol 32:4–13. CrossRefPubMedGoogle Scholar
  55. Ma MZ, Christensen MJ, Nan ZB (2015) Effects of the endophyte Epichloë festucae var. lolii of perennial ryegrass (Lolium perenne) on indicators of oxidative stress from pathogenic fungi during seed germination and seedling growth. Eur J Plant Pathol 141:571–583. CrossRefGoogle Scholar
  56. Maejima A, Saiga S, Inoue T, Tsuiki M (2000) Endophyte infection rate and alkaloid concentrations in seeds of commercial cultivars of perennial ryegrass. Jap J Grassl Sci 46:52–57Google Scholar
  57. Malinowski DP, Belesky DP (2010) Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassl Sci 52:1–14. CrossRefGoogle Scholar
  58. Mantri NL, Ford R, Coram TE, Pang ECK (2010) Evidence of unique and shared responses to major biotic and abiotic stresses in chickpea. Environ Exp Bot 69:286–292. CrossRefGoogle Scholar
  59. Megha S, Basu U, Kav NNV (2017) Regulation of low temperature stress in plants by microRNAs. Plant Cell Environ 41:1–15. CrossRefPubMedGoogle Scholar
  60. Mohammadian MA, Largani ZK, Sajedi RH (2012) Quantitative and qualitative comparison of antioxidant activity in the flavedo tissue of three cultivars of citrus fruit under cold stress. Aust J Crop Sci 6:402–406Google Scholar
  61. Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgeneration memory of stress in plants. Nature 442:1046–1049. CrossRefPubMedGoogle Scholar
  62. Munshaw GC, Ervin EH, Beasley JS, Shang C, Zhang X, Parrish DJ (2010) Effects of late-season ethephon applications on cold tolerance parameters of four bermudagrass cultivars. Crop Sci 50:1022–1029. CrossRefGoogle Scholar
  63. Murphy B, Martin-Nieto L, Doohan F, Hodkinson T (2015) Fungal endophytes enhance agronomically important traits in severely drought-stressed barley. J Agron Rop Sci 201:419–427. CrossRefGoogle Scholar
  64. Narra S (2007) Evaluation of sensing and machine vision techniques in stress detection and quality evaluation of turfgrass species. Thesis (Ph.D.): University of Illinois at Urbana-Champaign.
  65. Orabi SA, Salman SR, Shalaby MAF (2010) Increasing resistance to oxidative damage in cucumber (Cucumis sativus L.) plants by exogenous application of salicylic acid and paclobutrazol. World J Agric Sci 6:252–259Google Scholar
  66. Patchett B, Gooneratne R, Fletcher L, Chapman B (2011) Seasonal changes in leaf and stem loline alkaloids in meadow fescue. Crop Pasture Sci 62:261–267. CrossRefGoogle Scholar
  67. Pennell C, Rolston MP, Bonth AD, Simpson WR, Hume DE (2010) Development of a bird-deterrent fungal endophyte in turf tall fescue. N Z J Agr Res 53:145–150. CrossRefGoogle Scholar
  68. Qawasmeh A, Obied HK, Raman A, Wheatley W (2012) Influence of fungal endophyte infection on phenolic content and antioxidant activity in grasses: Interaction between Lolium perenne and different srains of Neotyphodium lolii. J Agric Food Chem 60:3381–3388. CrossRefPubMedGoogle Scholar
  69. Rasmussen S, Parsons AJ, Newman JA (2009) Metabolomics analysis of the Lolium perenne–Neotyphodium lolii symbiosis: more than just alkaloids? Phytochem Rev 8:535–550. CrossRefGoogle Scholar
  70. Redman RS, Yong OK, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6:e14823–e14833. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Rho H, Hsieh M, Kandel SL, Cantillo J, Doty SL, Kim SH (2017) Do endophytes promote growth of host plants under stress? A meta-analysis on plant stress mitigation by endophytes. Microb Ecol 75:1–12. CrossRefGoogle Scholar
  72. Richmond DS, Cardina J, Grewal PS (2006) Influence of grass species and endophyte infection on weed populations during establishment of low-maintenance lawns. Agric Ecosyst Environ 115:27–33. CrossRefGoogle Scholar
  73. Rodriguez R, Redman R (2007) More than 400 million years of evolution and some plants still can't make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 146:1109–1114. CrossRefGoogle Scholar
  74. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: A continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343. CrossRefGoogle Scholar
  75. Sanghera GS, Wani SH, Wasim H, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genomics 12:30–43. PMC 3129041
  76. Scebba F, Sebastiani L, Vitagliano C (1998) Changes in activity of antioxidative enzymes in wheat (Triticum aestivum) seedlings under cold acclimation. Physiol Plant 104:747–752. CrossRefGoogle Scholar
  77. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal wendophytes. Annu Rev Plant Biol 55:315–340. CrossRefPubMedGoogle Scholar
  78. Shao GC, Lan JJ, Yu SE, Liu N, Guo RQ, She DL (2013) Photosynthesis and growth of winter wheat in response to waterlogging at different growth stages. Photosynthetica 51:429–437. CrossRefGoogle Scholar
  79. Shen WY, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 124:431–439. CrossRefPubMedPubMedCentralGoogle Scholar
  80. Shimono H, Okada M, Kanda E, Arakawa I (2007) Low temperature-induced sterility in rice: Evidence for the effects of temperature before panicle initiation. Field Crop Res 101:221–231. CrossRefGoogle Scholar
  81. Siegel MR, Latch GCM, Johnson MC (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–297CrossRefGoogle Scholar
  82. Smith D (1951) Root branching of alfalfa varieties and strains6. Agron J 43:573–573CrossRefGoogle Scholar
  83. Song ML, Chai Q, Li XZ, Yao X, Li CJ, Christensen MJ, Nan ZB (2015) An asexual Epichloë endophyte modifies the nutrient stoichiometry of wild barley (Hordeum brevisubulatum) under salt stress. Plant Soil 387:153–165. CrossRefGoogle Scholar
  84. Svačina P, Středa T, Chloupek O (2014) Uncommon selection by root system size increases barley yield. Agron Sustain Dev 34:545–551. CrossRefGoogle Scholar
  85. Urbatzka P, Graß R, Haase T, Schüler C, Heß J (2012) Influence of different sowing dates of winter pea genotypes on winter hardiness and productivity as either winter catch crop or seed legume. Eur J Agron 40:112–119. CrossRefGoogle Scholar
  86. Vestena S, Cambraia J, Ribeiro C, Oliveira JA, Oliva MA (2011) Cadmium-induced oxidative stress and antioxidative enzyme response in water hyacinth and salvinia. Braz J Plant Physiol 23:131–139. CrossRefGoogle Scholar
  87. Viswanathan C, Zhu JH, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451. CrossRefGoogle Scholar
  88. Wang HF, He GX, Wang JH, Dong YY (2012) Monitoring winter wheat freeze injury based on multi-temporal data. Intell Autom Soft Co 18:1035–1042. CrossRefGoogle Scholar
  89. Wheatley WM, Kemp HW, Simpson WR, Hume DE, Nicol HI, Kemp DR, Launders TE (2007) Viability of endemic endophyte (Neotyphodium lolii) and perennial ryegrass (Lolium perenne) seed at retail and wholesale outlets in south-eastern Australia. Seed Sci Technol 35:360–370. CrossRefGoogle Scholar
  90. White JF, Sullivan RF, Moy M, Meyer W, Cabral D (2001) Evolution of Epichloë/ Neotyphodium endophytes and other clavicipitalean biotrophs. Symbiosis: Mechanisms and Model Systems (Cellular Origin, Life in Extreme Habitats and Astrobiology).
  91. Xin Z, Browse J (2010) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902. CrossRefGoogle Scholar
  92. Yarzábal LA (2014) Cold-tolerant phosphate-solubilizing microorganisms and agriculture development in mountainous regions of the world. 113–137. Google Scholar
  93. Young CA, Hume DE, Mcculley RL (2013) Forages and pastures aymposium: fungal endophytes of tall fescue and perennial ryegrass: Pasture friend or foe? J Anim Sci 91:2379–2394. CrossRefPubMedGoogle Scholar
  94. Yves C, RéAl M, Paul N, Annick B (2009) An indoor screening method for improvement of freezing tolerance in alfalfa. Crop Sci 49:809–818. CrossRefGoogle Scholar
  95. Zhang DF, Li FQ, Bing JM (2000) Eco-environmental effects of the Qinghai-Tibet Plateau uplift during the Quaternary in China. Environ Geol 39:1352–1358. CrossRefGoogle Scholar
  96. Zhang XX, Li CJ, Nan ZB (2010) Effects of cadmium stress on growth and anti-oxidative systems in Achnatherum inebrians symbiotic with Neotyphodium gansuense. J Hazard Mater 175:703–709. CrossRefPubMedGoogle Scholar
  97. Zhang XQ, Huang GQ, Huang ZL, Bian XM, Jiang XH (2012) Effects of low temperature on freezing injury of various winter wheat cultivars at different sowing time. Agric Sci Technol: English Edn 13:2332–2337Google Scholar
  98. Zhang T, Zhang YQ, Liu HY, Wei YZ, Li HL, Su J, Zhao LX, Yu LY (2013) Diversity and cold adaptation of culturable endophytic fungi from bryophytes in the Fildes Region, King George Island, maritime Antarctica. FEMS Microbiol Lett 341:52–61. CrossRefPubMedGoogle Scholar
  99. Zheng GW, Li LX, Li WQ (2016) Glycerolipidome responses to freezing- and chilling-induced injuries: examples in Arabidopsis and rice. BMC Plant Biol 16:70–85. CrossRefPubMedPubMedCentralGoogle Scholar
  100. Zhou LY, Li CJ, Zhang XX, Johnson R, Bao GS, Yao X, Chai Q (2015) Effects of cold shocked Epichloë infected Festuca sinensis on ergot alkaloid accumulation. Fungal Ecol 14:99–104. CrossRefGoogle Scholar
  101. Żurek M, Wiewióra B, Żurek G, Prończuk M (2012) Occurrence of endophyte fungi on grasses in Poland–Review. Fungal Ecol 5:353–356. CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; Engineering Research Center of Grassland Industry, Ministry of Education; Gansu Tech Innovation Center of Western China Grassland Industry; College of Pastoral Agriculture Science and TechnologyLanzhou UniversityLanzhouChina
  2. 2.Department of Plant BiologyRutgers UniversityNew BrunswickUSA

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